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Flow-mediated olfactory communication in honeybee swarms.

ABSTRACT: Honeybee swarms are a landmark example of collective behavior. To become a coherent swarm, bees locate their queen by tracking her pheromones. But how can distant individuals exploit these chemical signals, which decay rapidly in space and time? Here, we combine a behavioral assay with the machine vision detection of organism location and scenting (pheromone propagation via wing fanning) behavior to track the search and aggregation dynamics of the honeybee Apis mellifera L. We find that bees collectively create a scenting-mediated communication network by arranging in a specific spatial distribution where there is a characteristic distance between individuals and directional signaling away from the queen. To better understand such a flow-mediated directional communication strategy, we developed an agent-based model where bee agents obeying simple, local behavioral rules exist in a flow environment in which the chemical signals diffuse and decay. Our model serves as a guide to exploring how physical parameters affect the collective scenting behavior and shows that increased directional bias in scenting leads to a more efficient aggregation process that avoids local equilibrium configurations of isotropic (nondirectional and axisymmetric) communication, such as small bee clusters that persist throughout the simulation. Our results highlight an example of extended classical stigmergy: Rather than depositing static information in the environment, individual bees locally sense and globally manipulate the physical fields of chemical concentration and airflow.

SUBMITTER: Nguyen DMT

PROVIDER: S-EPMC8020754 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundSocial insect colonies routinely face large vertebrate predators, against which they need to mount a collective defence. To do so, honeybees use an alarm pheromone that recruits nearby bees into mass stinging of the perceived threat. This alarm pheromone is carried directly on the stinger; hence, its concentration builds up during the course of the attack. We investigate how bees react to different alarm pheromone concentrations and how this evolved response pattern leads to better coordination at the group level.ResultsWe first present a dose-response curve to the alarm pheromone, obtained experimentally. This data reveals two phases in the bees' response: initially, bees become more likely to sting as the alarm pheromone concentration increases, but aggressiveness drops back when very high concentrations are reached. Second, we apply Projective Simulation to model each bee as an artificial learning agent that relies on the pheromone concentration to decide whether to sting or not. Individuals are rewarded based on the collective performance, thus emulating natural selection in these complex societies. By also modelling predators in a detailed way, we are able to identify the main selection pressures that shaped the response pattern observed experimentally. In particular, the likelihood to sting in the absence of alarm pheromone (starting point of the dose-response curve) is inversely related to the rate of false alarms, such that bees in environments with low predator density are less likely to waste efforts responding to irrelevant stimuli. This is compensated for by a steep increase in aggressiveness when the alarm pheromone concentration starts rising. The later decay in aggressiveness may be explained as a curbing mechanism preventing worker loss.ConclusionsOur work provides a detailed understanding of alarm pheromone responses in honeybees and sheds light on the selection pressures that brought them about. In addition, it establishes our approach as a powerful tool to explore how selection based on a collective outcome shapes individual responses, which remains a challenging issue in the field of evolutionary biology.

Project description:The sensitivity of neurons from the honey bee olfactory system to pyrethroid insecticides was studied using the patch-clamp technique on central 'antennal lobe neurons' (ALNs) in cell culture. In these neurons, the voltage-dependent sodium currents are characterized by negative potential for activation, fast kinetics of activation and inactivation, and the presence of cumulative inactivation during train of depolarizations. Perfusion of pyrethroids on these ALN neurons submitted to repetitive stimulations induced (1) an acceleration of cumulative inactivation, and (2) a marked slowing of the tail current recorded upon repolarization. Cypermethrin and permethrin accelerated cumulative inactivation of the sodium current peak in a similar manner and tetramethrin was even more effective. The slow-down of channel deactivation was markedly dependent on the type of pyrethroid. With cypermethrin, a progressive increase of the tail current amplitude along with successive stimulations reveals a traditionally described use-dependent recruitment of modified sodium channels. However, an unexpected decrease in this tail current was revealed with tetramethrin. If one considers the calculated percentage of modified channels as an index of pyrethroids effects, ALNs are significantly more susceptible to tetramethrin than to permethrin or cypermethrin for a single depolarization, but this difference attenuates with repetitive activity. Further comparison with peripheral neurons from antennae suggest that these modifications are neuron type specific. Modeling the sodium channel as a multi-state channel with fast and slow inactivation allows to underline the effects of pyrethroids on a set of rate constants connecting open and inactivated conformations, and give some insights to their specificity. Altogether, our results revealed a differential sensitivity of central olfactory neurons to pyrethroids that emphasize the ability for these compounds to impair detection and processing of information at several levels of the bees olfactory pathway.

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Flow-mediated olfactory communication in honeybee swarms.

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